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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Different functions of biogenesis of lysosomal organelles complex 3 subunit 1 (Hps1) and adaptor-related protein complex 3, beta 1 subunit (Ap3b1) genes on spermatogenesis and male fertility

Renwei Jing A B , Haiqing Zhang C , Yu Kong A B , Kailin Li B E , Xuan Dong B , Jie Yan B , Jia Han D F and Lijun Feng https://orcid.org/0000-0002-7545-3122 B F
+ Author Affiliations
- Author Affiliations

A Basic Medical College, Tianjin Medical University, Qixiangtai Road, Heping District, Tianjin 300070, PR China.

B Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology, Institute of Developmental Biology, School of Life Sciences, Shandong University, Jinan, Shandong 250100, PR China.

C Department of Bioengineering, Shandong Polytechnic, Jinan, Shandong 250014, PR China.

D Department of Nephrology, Key Laboratory for Kidney Regeneration of Shandong Province, Shandong Provincial Hospital Affiliated to Shandong University, 324 Jingwu Street, Jinan, 250021, China.

E Present address: Central Research Laboratory, The Second Hospital of Shandong University, Jinan 250100, PR China.

F Corresponding authors. Emails: drfeng@sdu.edu.cn; macromidia@163.com

Reproduction, Fertility and Development 31(5) 972-982 https://doi.org/10.1071/RD18339
Submitted: 22 August 2018  Accepted: 24 December 2018   Published: 21 February 2019

Abstract

Hermansky–Pudlak syndrome (HPS) is an autosomal recessive disorder in humans and mice. Pale ear (ep) and pearl (pe) mice, bearing mutations in the biogenesis of lysosomal organelles complex 3 subunit 1 (Hps1) and adaptor-related protein complex 3, beta 1 subunit (Ap3b1) genes respectively, are mouse models of human HPS Type 1 (HPS1) and Type 2 (HPS2) respectively. In the present study we investigated and compared the reduced fertilities of ep and pe male mice. Both ep and pe males exhibited lower abilities to impregnate C57BL/6J (B6) females, and B6 females mated with ep males produced smaller litters than those mated with pe males. Delayed testis development, reduced sperm count and lower testosterone concentrations were observed in the pe but not ep male mice. However, the reduction in sperm motility was greater in ep than pe males, likely due to the mitochondrial and fibrous sheath abnormalities observed by electron microscopy in the sperm tails of ep males. Together, the results indicate that the Hps1 and Ap3b1 genes play distinct roles in male reproductive system development and spermatogenesis in mice, even though ep and pe males share common phenotypes, including reduced lysosomes in Sertoli cells and dislocated Zn2+ in sperm heads.

Additional keywords: acrosome, mitochondrial, Sertoli cell, sperm, testis, Zn2+.


References

Alto, N. M., Soderling, J., and Scott, J. D. (2002). Rab32 is an A-kinase anchoring protein and participates in mitochondrial dynamics. J. Cell Biol. 158, 659–668.
Rab32 is an A-kinase anchoring protein and participates in mitochondrial dynamics.Crossref | GoogleScholarGoogle Scholar | 12186851PubMed |

Atochina-Vasserman, E. N., Bates, S. R., Zhang, P., Abramova, H., Zhang, Z., Gonzales, L., Tao, J. Q., Gochuico, B. R., Gahl, W., Guo, C. J., Gow, A. J., Beers, M. F., and Guttentag, S. (2011). Early alveolar epithelial dysfunction promotes lung inflammation in a mouse model of Hermansky–Pudlak syndrome. Am. J. Respir. Crit. Care Med. 184, 449–458.
Early alveolar epithelial dysfunction promotes lung inflammation in a mouse model of Hermansky–Pudlak syndrome.Crossref | GoogleScholarGoogle Scholar | 21616998PubMed |

Badolato, R., and Parolini, S. (2007). Novel insights from adaptor protein 3 complex deficiency. J. Allergy Clin. Immunol. 120, 735–741.
Novel insights from adaptor protein 3 complex deficiency.Crossref | GoogleScholarGoogle Scholar | 17931556PubMed |

Becka, S., Zhang, P., Craig, S. E., Lodowski, D. T., Wang, Z., and Brady-Kalnay, S. M. (2010). Characterization of the adhesive properties of the Type IIb subfamily receptor protein tyrosine phosphatases. Cell Commun. Adhes. 17, 34–47.
Characterization of the adhesive properties of the Type IIb subfamily receptor protein tyrosine phosphatases.Crossref | GoogleScholarGoogle Scholar | 20521994PubMed |

Berruti, G. (2016). Towards defining an ‘origin’ – the case for the mammalian acrosome. Semin. Cell Dev. Biol. 59, 46–53.
Towards defining an ‘origin’ – the case for the mammalian acrosome.Crossref | GoogleScholarGoogle Scholar | 26775129PubMed |

Bultema, J. J., and Di Pietro, S. M. (2013). Cell type-specific Rab32 and Rab38 cooperate with the ubiquitous lysosome biogenesis machinery to synthesize specialized lysosome-related organelles. Small GTPases 4, 16–21.
Cell type-specific Rab32 and Rab38 cooperate with the ubiquitous lysosome biogenesis machinery to synthesize specialized lysosome-related organelles.Crossref | GoogleScholarGoogle Scholar | 23247405PubMed |

Bultema, J. J., Boyle, J. A., Malenke, P. B., Martin, F. E., Dell’Angelica, E. C., Cheney, R. E., and Di Pietro, S. M. (2014). Myosin vc interacts with Rab32 and Rab38 proteins and works in the biogenesis and secretion of melanosomes. J. Biol. Chem. 289, 33513–33528.
Myosin vc interacts with Rab32 and Rab38 proteins and works in the biogenesis and secretion of melanosomes.Crossref | GoogleScholarGoogle Scholar | 25324551PubMed |

Carmona-Rivera, C., Hess, R. A., O’Brien, K., Golas, G., Tsilou, E., White, J. G., Gahl, W. A., and Huizing, M. (2011). Novel mutations in the HPS1 gene among Puerto Rican patients. Clin. Genet. 79, 561–567.
Novel mutations in the HPS1 gene among Puerto Rican patients.Crossref | GoogleScholarGoogle Scholar | 20662851PubMed |

Chang, H., Gao, F., Guillou, F., Taketo, M. M., Huff, V., and Behringer, R. R. (2008). Wt1 negatively regulates beta-catenin signaling during testis development. Development 135, 1875–1885.
Wt1 negatively regulates beta-catenin signaling during testis development.Crossref | GoogleScholarGoogle Scholar | 18403409PubMed |

Chiang, P. W., Oiso, N., Gautam, R., Suzuki, T., Swank, R. T., and Spritz, R. A. (2003). The Hermansky–Pudlak syndrome 1 (HPS1) and HPS4 proteins are components of two complexes, BLOC-3 and BLOC-4, involved in the biogenesis of lysosome-related organelles. J. Biol. Chem. 278, 20332–20337.
The Hermansky–Pudlak syndrome 1 (HPS1) and HPS4 proteins are components of two complexes, BLOC-3 and BLOC-4, involved in the biogenesis of lysosome-related organelles.Crossref | GoogleScholarGoogle Scholar | 12663659PubMed |

Colagar, A. H., Marzony, E. T., and Chaichi, M. J. (2009). Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr. Res. 29, 82–88.
Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men.Crossref | GoogleScholarGoogle Scholar | 19285597PubMed |

de Boer, M., van Leeuwen, K., Geissler, J., van Alphen, F., de Vries, E., van der Kuip, M., Terheggen, S. W. J., Janssen, H., van den Berg, T. K., Meijer, A. B., Roos, D., and Kuijpers, T. W. (2017). Hermansky–Pudlak syndrome type 2: aberrant pre-mRNA splicing and mislocalization of granule proteins in neutrophils. Hum. Mutat. 38, 1402–1411.
Hermansky–Pudlak syndrome type 2: aberrant pre-mRNA splicing and mislocalization of granule proteins in neutrophils.Crossref | GoogleScholarGoogle Scholar | 28585318PubMed |

Dell’Angelica, E. C., Shotelersuk, V., Aguilar, R. C., Gahl, W. A., and Bonifacino, J. S. (1999). Altered trafficking of lysosomal proteins in Hermansky–Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell 3, 11–21.
Altered trafficking of lysosomal proteins in Hermansky–Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor.Crossref | GoogleScholarGoogle Scholar | 10024875PubMed |

Dennis, M. K., Delevoye, C., Acosta-Ruiz, A., Hurbain, I., Romao, M., Hesketh, G. G., Goff, P. S., Sviderskaya, E. V., Bennett, D. C., Luzio, J. P., Galli, T., Owen, D. J., Raposo, G., and Marks, M. S. (2016). BLOC-1 and BLOC-3 regulate VAMP7 cycling to and from melanosomes via distinct tubular transport carriers. J. Cell Biol. 214, 293–308.
BLOC-1 and BLOC-3 regulate VAMP7 cycling to and from melanosomes via distinct tubular transport carriers.Crossref | GoogleScholarGoogle Scholar | 27482051PubMed |

Dong, H., Yuan, H., Jin, W., Shen, Y., Xu, X., and Wang, H. (2007). Involvement of beta3A subunit of adaptor protein-3 in intracellular trafficking of receptor-like protein tyrosine phosphatase PCP-2. Acta Biochim. Biophys. Sin. (Shanghai) 39, 540–546.
Involvement of beta3A subunit of adaptor protein-3 in intracellular trafficking of receptor-like protein tyrosine phosphatase PCP-2.Crossref | GoogleScholarGoogle Scholar | 17622474PubMed |

El-Chemaly, S., and Young, L. R. (2016). Hermansky–Pudlak syndrome. Clin. Chest Med. 37, 505–511.
Hermansky–Pudlak syndrome.Crossref | GoogleScholarGoogle Scholar | 27514596PubMed |

Feng, G. H., Bailin, T., Oh, J., and Spritz, R. A. (1997). Mouse pale ear (ep) is homologous to human Hermansky–Pudlak syndrome and contains a rare ‘AT–AC’ intron. Hum. Mol. Genet. 6, 793–797.
Mouse pale ear (ep) is homologous to human Hermansky–Pudlak syndrome and contains a rare ‘AT–AC’ intron.Crossref | GoogleScholarGoogle Scholar | 9158155PubMed |

Feng, L., Seymour, A. B., Jiang, S., To, A., Peden, A. A., Novak, E. K., Zhen, L., Rusiniak, M. E., Eicher, E. M., Robinson, M. S., Gorin, M. B., and Swank, R. T. (1999). The beta3A subunit gene (Ap3b1) of the AP-3 adaptor complex is altered in the mouse hypopigmentation mutant pearl, a model for Hermansky–Pudlak syndrome and night blindness. Hum. Mol. Genet. 8, 323–330.
The beta3A subunit gene (Ap3b1) of the AP-3 adaptor complex is altered in the mouse hypopigmentation mutant pearl, a model for Hermansky–Pudlak syndrome and night blindness.Crossref | GoogleScholarGoogle Scholar | 9931340PubMed |

Feng, L., Novak, E. K., Hartnell, L. M., Bonifacino, J. S., Collinson, L. M., and Swank, R. T. (2002). The Hermansky–Pudlak syndrome 1 (HPS1) and HPS2 genes independently contribute to the production and function of platelet dense granules, melanosomes, and lysosomes. Blood 99, 1651–1658.
| 11861280PubMed |

Gautam, R., Novak, E. K., Tan, J., Wakamatsu, K., Ito, S., and Swank, R. T. (2006). Interaction of Hermansky–Pudlak syndrome genes in the regulation of lysosome-related organelles. Traffic 7, 779–792.
Interaction of Hermansky–Pudlak syndrome genes in the regulation of lysosome-related organelles.Crossref | GoogleScholarGoogle Scholar | 16787394PubMed |

Gerondopoulos, A., Langemeyer, L., Liang, J. R., Linford, A., and Barr, F. A. (2012). BLOC-3 mutated in Hermansky–Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor. Curr. Biol. 22, 2135–2139.
BLOC-3 mutated in Hermansky–Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor.Crossref | GoogleScholarGoogle Scholar | 23084991PubMed |

Haile, Y., Deng, X., Ortiz-Sandoval, C., Tahbaz, N., Janowicz, A., Lu, J. Q., Kerr, B. J., Gutowski, N. J., Holley, J. E., Eggleton, P., Giuliani, F., and Simmen, T. (2017). Rab32 connects ER stress to mitochondrial defects in multiple sclerosis. J. Neuroinflammation 14, 19.
Rab32 connects ER stress to mitochondrial defects in multiple sclerosis.Crossref | GoogleScholarGoogle Scholar | 28115010PubMed |

Hermansky, F., and Pudlak, P. (1959). Albinism associated with hemorrhagic diathesis and unusual pigmented reticular cells in the bone marrow: report of two cases with histochemical studies. Blood 14, 162–169.
| 13618373PubMed |

Huizing, M., Scher, C. D., Strovel, E., Fitzpatrick, D. L., Hartnell, L. M., Anikster, Y., and Gahl, W. A. (2002). Nonsense mutations in ADTB3A cause complete deficiency of the beta3A subunit of adaptor complex-3 and severe Hermansky–Pudlak syndrome type 2. Pediatr. Res. 51, 150–158.
Nonsense mutations in ADTB3A cause complete deficiency of the beta3A subunit of adaptor complex-3 and severe Hermansky–Pudlak syndrome type 2.Crossref | GoogleScholarGoogle Scholar | 11809908PubMed |

Huizing, M., Helip-Wooley, A., Westbroek, W., Gunay-Aygun, M., and Gahl, W. A. (2008). Disorders of lysosome-related organelle biogenesis: clinical and molecular genetics. Annu. Rev. Genomics Hum. Genet. 9, 359–386.
Disorders of lysosome-related organelle biogenesis: clinical and molecular genetics.Crossref | GoogleScholarGoogle Scholar | 18544035PubMed |

Ishida, M., Oguchi, M. E., and Fukuda, M. (2016). Multiple types of guanine nucleotide exchange factors (GEFs) for Rab small GTPases. Cell Struct. Funct. 41, 61–79.
Multiple types of guanine nucleotide exchange factors (GEFs) for Rab small GTPases.Crossref | GoogleScholarGoogle Scholar | 27246931PubMed |

Jamsai, D., and O’Bryan, M. K. (2011). Mouse models in male fertility research. Asian J. Androl. 13, 139–151.
Mouse models in male fertility research.Crossref | GoogleScholarGoogle Scholar | 21057516PubMed |

Jardón, J., Izquierdo, N. J., Renta, J. Y., García-Rodríguez, O., and Cadilla, C. L. (2016). Ocular findings in patients with the Hermansky–Pudlak syndrome (Types 1 and 3). Ophthalmic Genet. 37, 89–94.
| 24766090PubMed |

Jing, R., Dong, X., Li, K., Yan, J., Chen, X., and Feng, L. (2014). The Ap3b1 gene regulates the ocular melanosome biogenesis and tyrosinase distribution differently from the Hps1 gene. Exp. Eye Res. 128, 57–66.
The Ap3b1 gene regulates the ocular melanosome biogenesis and tyrosinase distribution differently from the Hps1 gene.Crossref | GoogleScholarGoogle Scholar | 25160823PubMed |

Kantheti, P., Qiao, X., Diaz, M. E., Peden, A. A., Meyer, G. E., Carskadon, S. L., Kapfhamer, D., Sufalko, D., Robinson, M. S., Noebels, J. L., and Burmeister, M. (1998). Mutation in AP-3 delta in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron 21, 111–122.
Mutation in AP-3 delta in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles.Crossref | GoogleScholarGoogle Scholar | 9697856PubMed |

Kerns, K., Zigo, M., Drobnis, E. Z., Sutovsky, M., and Sutovsky, P. (2018). Zinc ion flux during mammalian sperm capacitation. Nat. Commun. 9, 2061.
Zinc ion flux during mammalian sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 29802294PubMed |

Khan, A. O., Tamimi, M., Lenzner, S., and Bolz, H. J. (2016). Hermansky–Pudlak syndrome genes are frequently mutated in patients with albinism from the Arabian Peninsula. Clin. Genet. 90, 96–98.
Hermansky–Pudlak syndrome genes are frequently mutated in patients with albinism from the Arabian Peninsula.Crossref | GoogleScholarGoogle Scholar | 26785811PubMed |

Kloer, D. P., Rojas, R., Ivan, V., Moriyama, K., van Vlijmen, T., Murthy, N., Ghirlando, R., van der Sluijs, P., Hurley, J. H., and Bonifacino, J. S. (2010). Assembly of the biogenesis of lysosome-related organelles complex-3 (BLOC-3) and its interaction with Rab9. J. Biol. Chem. 285, 7794–7804.
Assembly of the biogenesis of lysosome-related organelles complex-3 (BLOC-3) and its interaction with Rab9.Crossref | GoogleScholarGoogle Scholar | 20048159PubMed |

Kook, S., Wang, P., Young, L. R., Schwake, M., Saftig, P., Weng, X., Meng, Y., Neculai, D., Marks, M. S., Gonzales, L., Beers, M. F., and Guttentag, S. (2016). Impaired lysosomal integral membrane protein 2-dependent peroxiredoxin 6 delivery to lamellar bodies accounts for altered alveolar phospholipid content in adaptor protein-3-deficient pearl mice. J. Biol. Chem. 291, 8414–8427.
Impaired lysosomal integral membrane protein 2-dependent peroxiredoxin 6 delivery to lamellar bodies accounts for altered alveolar phospholipid content in adaptor protein-3-deficient pearl mice.Crossref | GoogleScholarGoogle Scholar | 26907692PubMed |

Lewis-Jones, D. I., Aird, I. A., Biljan, M. M., and Kingsland, C. R. (1996). Effects of sperm activity on zinc and fructose concentrations in seminal plasma. Hum. Reprod. 11, 2465–2467.
Effects of sperm activity on zinc and fructose concentrations in seminal plasma.Crossref | GoogleScholarGoogle Scholar | 8981134PubMed |

Li, Y., Zhang, L., Hu, Y., Chen, M., Han, F., Qin, Y., Chen, M., Cui, X., Duo, S., Tang, F., and Gao, F. (2017). β-Catenin directs the transformation of testis Sertoli cells to ovarian granulosa-like cells by inducing Foxl2 expression. J. Biol. Chem. 292, 17577–17586.
β-Catenin directs the transformation of testis Sertoli cells to ovarian granulosa-like cells by inducing Foxl2 expression.Crossref | GoogleScholarGoogle Scholar | 28900034PubMed |

Ma, J., Zhang, Z., Yang, L., Kriston-Vizi, J., Cutler, D. F., and Li, W. (2016). BLOC-2 subunit HPS6 deficiency affects the tubulation and secretion of von Willebrand factor from mouse endothelial cells. J. Genet. Genomics 43, 686–693.
BLOC-2 subunit HPS6 deficiency affects the tubulation and secretion of von Willebrand factor from mouse endothelial cells.Crossref | GoogleScholarGoogle Scholar | 27889498PubMed |

Mahran, A. M., Elgamal, D. A., Ghafeer, H. H., Abdel-Maksoud, S. A., and Farrag, A. A. (2017). Histological alterations in Leydig cells and macrophages in azoospermic men. Andrologia 49, e12714.
Histological alterations in Leydig cells and macrophages in azoospermic men.Crossref | GoogleScholarGoogle Scholar | 27709649PubMed |

Mantegazza, A. R., Guttentag, S. H., El-Benna, J., Sasai, M., Iwasaki, A., Shen, H., Laufer, T. M., and Marks, M. S. (2012). Adaptor protein-3 in dendritic cells facilitates phagosomal toll-like receptor signaling and antigen presentation to CD4(+) T cells. Immunity 36, 782–794.
Adaptor protein-3 in dendritic cells facilitates phagosomal toll-like receptor signaling and antigen presentation to CD4(+) T cells.Crossref | GoogleScholarGoogle Scholar | 22560444PubMed |

Mao, G. F., Goldfinger, L. E., Fan, D. C., Lambert, M. P., Jalagadugula, G., Freishtat, R., and Rao, A. K. (2017). Dysregulation of PLDN (pallidin) is a mechanism for platelet dense granule deficiency in RUNX1 haplodeficiency. J. Thromb. Haemost. 15, 792–801.
Dysregulation of PLDN (pallidin) is a mechanism for platelet dense granule deficiency in RUNX1 haplodeficiency.Crossref | GoogleScholarGoogle Scholar | 28075530PubMed |

Sakai, Y., Nakamoto, T., and Yamashina, S. (1988). Dynamic changes in Sertoli cell processes invading spermatid cytoplasm during mouse spermiogenesis. Anat. Rec. 220, 51–57.
Dynamic changes in Sertoli cell processes invading spermatid cytoplasm during mouse spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 2964797PubMed |

Sánchez-Guiu, I., Torregrosa, J. M., Velasco, F., Antón, A. I., Lozano, M. L., Vicente, V., and Rivera, J. (2014). Hermansky–Pudlak syndrome. Overview of clinical and molecular features and case report of a new HPS1 variant. Hamostaseologie 34, 301–309.
Hermansky–Pudlak syndrome. Overview of clinical and molecular features and case report of a new HPS1 variant.Crossref | GoogleScholarGoogle Scholar | 25117010PubMed |

Skakkebaek, N. E., Rajpert-De Meyts, E., Buck Louis, G. M., Toppari, J., Andersson, A. M., Eisenberg, M. L., Jensen, T. K., Jørgensen, N., Swan, S. H., Sapra, K. J., Ziebe, S., Priskorn, L., and Juul, A. (2016). Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility. Physiol. Rev. 96, 55–97.
Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility.Crossref | GoogleScholarGoogle Scholar | 26582516PubMed |

Spritz, R. A. (2000). Hermansky–Pudlak syndrome and pale ear: melanosome-making for the millennium. Pigment Cell Res. 13, 15–20.
Hermansky–Pudlak syndrome and pale ear: melanosome-making for the millennium.Crossref | GoogleScholarGoogle Scholar | 10761991PubMed |

Swank, R. T., Novak, E. K., McGarry, M. P., Rusiniak, M. E., and Feng, L. (1998). Mouse models of Hermansky–Pudlak syndrome: a review. Pigment Cell Res. 11, 60–80.
Mouse models of Hermansky–Pudlak syndrome: a review.Crossref | GoogleScholarGoogle Scholar | 9585243PubMed |

Tanwar, P. S., Kaneko-Tarui, T., Zhang, L., Rani, P., Taketo, M. M., and Teixeira, J. (2010). Constitutive WNT/beta-catenin signaling in murine Sertoli cells disrupts their differentiation and ability to support spermatogenesis. Biol. Reprod. 82, 422–432.
Constitutive WNT/beta-catenin signaling in murine Sertoli cells disrupts their differentiation and ability to support spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 19794154PubMed |

Vicary, G. W., Vergne, Y., Santiago-Cornier, A., Rani, P., Taketo, M. M., and Teixeira, J. (2016). Pulmonary fibrosis in Hermansky–Pudlak syndrome. Ann. Am. Thorac. Soc. 13, 1839–1846.
| 27529121PubMed |

Wei, M. L. (2006). Hermansky–Pudlak syndrome: a disease of protein trafficking and organelle function. Pigment Cell Res. 19, 19–42.
Hermansky–Pudlak syndrome: a disease of protein trafficking and organelle function.Crossref | GoogleScholarGoogle Scholar | 16420244PubMed |

Wei, A. H., and Li, W. (2013). Hermansky–Pudlak syndrome: pigmentary and non-pigmentary defects and their pathogenesis. Pigment Cell Melanoma Res. 26, 176–192.
Hermansky–Pudlak syndrome: pigmentary and non-pigmentary defects and their pathogenesis.Crossref | GoogleScholarGoogle Scholar | 23171219PubMed |

Yan, H. X., He, Y. Q., Dong, H., Zhang, P., Zeng, J. Z., Cao, H. F., Wu, M. C., and Wang, H. Y. (2002). Physical and functional interaction between receptor-like protein tyrosine phosphatase PCP-2 and beta-catenin. Biochemistry 41, 15854–15860.
Physical and functional interaction between receptor-like protein tyrosine phosphatase PCP-2 and beta-catenin.Crossref | GoogleScholarGoogle Scholar | 12501215PubMed |

Yan, H. X., Yang, W., Zhang, R., Chen, L., Tang, L., Zhai, B., Liu, S. Q., Cao, H. F., Man, X. B., Wu, H. P., Wu, M. C., and Wang, H. Y. (2006). Protein-tyrosine phosphatase PCP-2 inhibits beta-catenin signaling and increases E-cadherin-dependent cell adhesion. J. Biol. Chem. 281, 15423–15433.
Protein-tyrosine phosphatase PCP-2 inhibits beta-catenin signaling and increases E-cadherin-dependent cell adhesion.Crossref | GoogleScholarGoogle Scholar | 16574648PubMed |

Young, L. R., Borchers, M. T., Allen, H. L., Gibbons, R. S., and McCormack, F. X. (2006). Lung-restricted macrophage activation in the pearl mouse model of Hermansky–Pudlak syndrome. J. Immunol. 176, 4361–4368.
Lung-restricted macrophage activation in the pearl mouse model of Hermansky–Pudlak syndrome.Crossref | GoogleScholarGoogle Scholar | 16547274PubMed |

Zalewski, P. D., Jian, X., Soon, L. L., Breed, W. G., Seamark, R. F., Lincoln, S. F., Ward, A. D., and Sun, F. Z. (1996). Changes in distribution of labile zinc in mouse spermatozoa during maturation in the epididymis assessed by the fluorophore Zinquin. Reprod. Fertil. Dev. 8, 1097–1105.
Changes in distribution of labile zinc in mouse spermatozoa during maturation in the epididymis assessed by the fluorophore Zinquin.Crossref | GoogleScholarGoogle Scholar | 8916286PubMed |